Identification of urinary metabolites that distinguish membranous lupus nephritis from proliferative lupus nephritis and focal segmental glomerulosclerosis

Arthritis Research and Therapy

Volumn 13, Issue 6, 2011, Pages

  Romick Rosendale, Lindsey E ^a   Brunner, Hermine I ^b   Bennett, Michael R ^b   Mina, Rina ^a   Nelson, Shannen ^b   Petri, Michelle ^c   Kiani, Adnan ^c   Devarajan, Prasad ^b   Kennedy, Michael A ^a  

^a MIAMI UNIVERSITY   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRIC ACID; HIPPURIC ACID; TAURINE; HIPPURIC ACID DERIVATIVE;

ADULT; ARTICLE; CHILD; CLINICAL ARTICLE; CLINICAL STUDY; CONTROLLED STUDY; DISEASE CLASSIFICATION; DISEASE CONTROL; FEMALE; FOCAL GLOMERULOSCLEROSIS; HUMAN; HUMAN TISSUE; KIDNEY BIOPSY; LUPUS ERYTHEMATOSUS NEPHRITIS; MALE; MEMBRANOUS LUPUS NEPHRITIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROLIFERATIVE LUPUS NEPHRITIS; PROTEINURIA; URINALYSIS; DIFFERENTIAL DIAGNOSIS; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MEMBRANOUS GLOMERULONEPHRITIS; METABOLISM; METABOLOMICS; METHODOLOGY; PILOT STUDY; PRINCIPAL COMPONENT ANALYSIS; RECEIVER OPERATING CHARACTERISTIC; SYSTEMIC LUPUS ERYTHEMATOSUS; URINE;

CITRIC ACID; DIAGNOSIS, DIFFERENTIAL; FEMALE; GLOMERULONEPHRITIS, MEMBRANOPROLIFERATIVE; GLOMERULONEPHRITIS, MEMBRANOUS; HIPPURATES; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; PILOT PROJECTS; PRINCIPAL COMPONENT ANALYSIS; ROC CURVE; TAURINE;

EID: 82755167807     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3530     Document Type: Article

References (60)

1. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997, 40:1725.
2. Chambers SA, Allen E, Rahman A, Isenberg D. Damage and mortality in a group of British patients with systemic lupus erythematosus followed up for over 10 years. Rheumatology (Oxford) 2009, 48:673-675.
3. Austin HA, Illei GG. Membranous lupus nephritis. Lupus 2005, 14:65-71. 10.1191/0961203305lu2062oa, 15732291.
4. Navaneethan SD, Viswanathan G, Strippoli GF. Treatment options for proliferative lupus nephritis: an update of clinical trial evidence. Drugs 2008, 68:2095-2104. 10.2165/00003495-200868150-00002, 18840001.
5. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol 2004, 15:241-250. 10.1097/01.ASN.0000108969.21691.5D, 14747370.
6. Rivera TL, Belmont HM, Malani S, Latorre M, Benton L, Weisstuch J, Barisoni L, Tseng CE, Izmirly PM, Buyon JP, Askanase AD. Current therapies for lupus nephritis in an ethnically heterogeneous cohort. J Rheumatol 2009, 36:298-305.
7. Mok CC. Membranous nephropathy in systemic lupus erythematosus: a therapeutic enigma. Nat Rev Nephrol 2009, 5:212-220. 10.1038/nrneph.2009.14, 19322186.
8. Mundel P, Shankland SJ. Podocyte biology and response to injury. J Am Soc Nephrol 2002, 13:3005-3015. 10.1097/01.ASN.0000039661.06947.FD, 12444221.
9. Das L, Brunner HI. Biomarkers for renal disease in childhood. Curr Rheumatol Rep 2009, 11:218-225. 10.1007/s11926-009-0030-4, 19604467.
10. Rovin BH, Birmingham DJ, Nagaraja HN, Yu CY, Hebert LA. Biomarker discovery in human SLE nephritis. Bull NYU Hosp Jt Dis 2007, 65:187-193.
11. Boudonck KJ, Rose DJ, Karoly ED, Lee DP, Lawton KA, Lapinskas PJ. Metabolomics for early detection of drug-induced kidney injury: review of the current status. Bioanalysis 2009, 1:1645-1663. 10.4155/bio.09.142, 21083109.
12. Kraly JR, Holcomb RE, Guan Q, Henry CS. Review: Microfluidic applications in metabolomics and metabolic profiling. Anal Chim Acta 2009, 653:23-35. 10.1016/j.aca.2009.08.037, 2791705, 19800473.
13. Nicholson JK, Wilson ID. High resolution proton magnetic resonance spectroscopy of biological fluids. Prog Nucl Magn Reson Spectrosc 1989, 21:449-501.
14. Lindon JC, Holmes E, Nicholson JK. Pattern recognition methods and applications in biomedical magnetic resonance. Prog Nucl Magn Reson Spectrosc 2001, 39:1-40.
15. Lindon JC, Nicholson JK, Holmes E, Everett JR. Metabonomics: Metabolic processes studied by NMR spectroscopy of biofluids. Concepts Magn Reson 2000, 12:289-320.
16. Park EM, Lee E, Joo HJ, Oh E, Lee J, Lee JS. Inter- and intra-individual variations of urinary endogenous metabolites in healthy male college students using H-1 NMR spectroscopy. Clin Chem Lab Med 2009, 47:188-194. 10.1515/CCLM.2009.040, 19191725.
17. Nicholson JK, Lindon JC, Holmes E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 1999, 29:1181-1189. 10.1080/004982599238047, 10598751.
18. Schwartz GJ, Haycock GB, Edelmann CM, Spitzer A. A simple estimate of glomerular filtration rate in children derived from body length and plasma creatinine. Pediatrics 1976, 58:259-263.
19. Kasitanon N, Fine DM, Haas M, Magder LS, Petri M. Estimating renal function in lupus nephritis: comparison of the Modification of Diet in Renal Disease and Cockcroft Gault equations. Lupus 2007, 16:887-895. 10.1177/0961203307084167, 17971362.
20. Austin HA, Muenz LR, Joyce KM, Antonovych TT, Balow JE. Diffuse proliferative lupus nephritis: identification of specific pathologic features affecting renal outcome. Kidney Int 1984, 25:689-695. 10.1038/ki.1984.75, 6482173.
21. Zappitelli M, Duffy CM, Bernard C, Gupta IR. Evaluation of activity, chronicity and tubulointerstitial indices for childhood lupus nephritis. Pediatr Nephrol 2008, 23:83-91.
22. Hiramatsu N, Kuroiwa T, Ikeuchi H, Maeshima A, Kaneko Y, Hiromura K, Ueki K, Nojima Y. Revised classification of lupus nephritis is valuable in predicting renal outcome with an indication of the proportion of glomeruli affected by chronic lesions. Rheumatology (Oxford) 2008, 47:702-707.
23. Cortés-Hernández J, Ordi-Ros J, Labrador M, Segarra A, Tovar JL, Balada E, Vilardell-Tarres M. Predictors of poor renal outcome in patients with lupus nephritis treated with combined pulses of cyclophosphamide and methylprednisolone. Lupus 2003, 12:287-296. 10.1191/0961203303lu340oa, 12729052.
24. Marks SD, Sebire NJ, Pilkington C, Tullus K. Clinicopathological correlations of paediatric lupus nephritis. Pediatr Nephrol 2007, 22:77-83. 10.1007/s00467-006-0296-y, 17106692.
25. Zappitelli M, Duffy C, Bernard C, Scuccimarri R, Watanabe Duffy K, Kagan R, Gupta IR. Clinicopathological study of the WHO classification in childhood lupus nephritis. Pediatr Nephrol 2004, 19:503-510. 10.1007/s00467-004-1419-y, 15022106.
26. Lee BS, Cho HY, Kim EJ, Kang HG, Ha IS, Cheong HI, Kim JG, Lee HS, Choi Y. Clinical outcomes of childhood lupus nephritis: a single center's experience. Pediatr Nephrol 2007, 22:222-231.
27. Demircin G, Oner A, Erdoǧan O, Delibaş A, Baysun S, Bülbül M, Bek K, Oksal A. Long-term efficacy and safety of quadruple therapy in childhood diffuse proliferative lupus nephritis. Ren Fail 2008, 30:603-609. 10.1080/08860220802132171, 18661410.
28. Vachvanichsanong P, Dissaneewate P, McNeil E. Diffuse proliferative glomerulonephritis does not determine the worst outcome in childhood-onset lupus nephritis: a 23-year experience in a single centre. Nephrol Dial Transplant 2009, 24:2729-2734. 10.1093/ndt/gfp173, 19395731.
29. Hagelberg S, Lee Y, Bargman J, Mah G, Schneider R, Laskin C, Eddy A, Gladman D, Urowitz M, Hebert D, Silverman E. Longterm followup of childhood lupus nephritis. J Rheumatol 2002, 29:2635-2642.
30. Hersh AO, von Scheven E, Yazdany J, Panopalis P, Trupin L, Julian L, Katz P, Criswell LA, Yelin E. Differences in long-term disease activity and treatment of adult patients with childhood- and adult-onset systemic lupus erythematosus. Arthritis Rheum 2009, 61:13-20. 2875186, 19116979.
31. Ibañez D, Gladman DD, Urowitz MB. Adjusted mean Systemic Lupus Erythematosus Disease Activity Index-2K is a predictor of outcome in SLE. J Rheumatol 2005, 32:824-827.
32. Gladman DD, Goldsmith CH, Urowitz MB, Bacon P, Fortin P, Ginzler E, Gordon C, Hanly JG, Isenberg DA, Petri M, Nived O, Snaith M, Sturfelt G. The Systemic Lupus International Collaborating Clinics/American College of Rheumatology (SLICC/ACR) Damage Index for Systemic Lupus Erythematosus International Comparison. J Rheumatol 2000, 27:373-376.
33. Rousseau R, Govaerts B, Verleysen M, Boulanger B. Comparison of some chemometric tools for metabonomics biomarker identification. Selected papers presented at the Chemometrics Congress "CHIMIOMETRIE 2006" Paris, France, 30 November - 1 December 2006, 91:54-66.
34. Goodpaster AM, Romick-Rosendale LE, Kennedy MA. Statistical significance analysis of nuclear magnetic resonance-based metabonomics data. Anal Biochem 2010, 401:134-143. 10.1016/j.ab.2010.02.005, 20159006.
35. Goodpaster AM, Kennedy MA. Quantification and statistical significance analysis of group separation in NMR-based metabonomics studies. Chemometr Intell Lab 2011, 109:162-170.
36. Statistics Calculator (version 3.0). , http://www.danielsoper.com/statcalc3/calc.aspx?id=4
37. Saude E, Adamko D, Rowe B, Marrie T, Sykes B. Variation of metabolites in normal human urine. Metabolomics 2007, 3:439-451.
38. Laidlaw SA, Shultz TD, Cecchino JT, Kopple JD. Plasma and urine taurine levels in vegans. Am J Clin Nutr 1988, 47:660-663.
39. Quaggin SE, Kreidberg JA. Development of the renal glomerulus: good neighbors and good fences. Development 2008, 135:609-620. 10.1242/dev.001081, 18184729.
40. Christians U, Schmitz V, Schöning W, Bendrick-Peart J, Klawitter J, Haschke M. Toxicodynamic therapeutic drug monitoring of immunosuppressants: promises, reality, and challenges. Ther Drug Monit 2008, 30:151-158. 10.1097/FTD.0b013e31816b9063, 18367974.
41. Clarke E, Evans BM, MacIntyre I, Milne MD. Acidosis in experimental electrolyte depletion. Clin Sci 1955, 14:421.
42. Morrissey JF, Ochoa M, Lotspeich WD, Waterhouse C. Citrate Excretion in Renal Tubular Acidosis. Ann Intern Med 1962, 56:697-698.
43. Unwin RJ, Capasso G, Shirley DG. An overview of divalent cation and citrate handling by the kidney. Nephron Physiol 2004, 98:15-20.
44. Melnick JZ, Preisig PA, Alpern RJ, Baum M. Renal citrate metabolism and urinary citrate excretion in the infant rat. Kidney Int 2000, 57:891-897. 10.1046/j.1523-1755.2000.057003891.x, 10720942.
45. Trachtman H, Sturman JA. Taurine: A therapeutic agent in experimental kidney disease. Amino Acids 1996, 11:1-13.
46. Sturman JA, Hepner GW, Hofmann AF, Thomas PJ. Metabolism of [35S]taurine in man. J Nutr 1975, 105:1206-1214.
47. Paauw JD, Davis AT. Taurine concentrations in serum of critically injured patients and age- and sex- matched healthy control subjects. Am J Clin Nutr 1990, 52:657-660.
48. Lourenco R, Camilo ME. Taurine: a conditionally essential amino acid in humans? An overview in health and disease. Nutr Hosp 2002, 17:262-270.
49. Yap IK, Angley M, Veselkov KA, Holmes E, Lindon JC, Nicholson JK. Urinary metabolic phenotyping differentiates children with autism from their unaffected siblings and age-matched controls. J Proteome Res 2010, 9:2996-3004. 10.1021/pr901188e, 20337404.
50. Cruz CI, Ruiz-Torres P, del Moral RG, Rodriguez-Puyol M, Rodriguez-Puyol D. Age-related progressive renal fibrosis in rats and its prevention with ACE inhibitors and taurine. Am J Physiol Renal Physiol 2000, 278:F122-129.
51. Yamori Y, Murakami S, Ikeda K, Nara Y. Fish and lifestyle-related disease prevention: experimental and epidemiological evidence for anti-atherogenic potential of taurine. Clin Exp Pharmacol Physiol 2004, 31(Suppl 2):S20-23.
52. Austin Iii HA, Muenz LR, Joyce KM, Antonovych TA, Kullick ME, Klippel JH, Decker JL, Balow JE. Prognostic factors in lupus nephritis: contribution of renal histologic data. Am J Med 1983, 75:382-391. 10.1016/0002-9343(83)90338-8, 6351607.
53. Wernick RM, Smith DL, Houghton DC, Phillips DS, Booth JL, Runckel DN, Johnson DS, Brown KK, Gaboury CL. Reliability of histologic scoring for lupus nephritis: a community-based evaluation. Ann Intern Med 1993, 119:805-811.
54. Pirani CL, Pollack VE, Schwartz FD. The reproducibility of semiquantitative analyses of renal histology. Nephron 1964, 1:230-237. 10.1159/000179336, 14263632.
55. Wallace DJ, Hahn B, Dubois EL. Dubois' lupus erythematosus 2007, Philadelphia: Lippincott Williams & Wilkin, 7.
56. Christopher-Stine L, Petri M, Astor BC, Fine D. Urine protein-to-creatinine ratio is a reliable measure of proteinuria in lupus nephritis. J Rheumatol 2004, 31:1557-1559.
57. Appel GB, Cohen DJ, Pirani CL, Meltzer JI, Estes D. Long-term follow-up of patients with lupus nephritis: A study based on the classification of the World Health Organization. Am J Med 1987, 83:877-885. 10.1016/0002-9343(87)90645-0, 3674094.
58. Schwartz MM, Bernstein J, Hill GS, Holley K, Phillips EA. Predictive value of renal pathology in diffuse proliferative lupus glomerulonephritis. Lupus Nephritis Collaborative Study Group. Kidney Int 1989, 36:891-896. 10.1038/ki.1989.276, 2615196.
59. Williams H, Cox IJ, Walker D, Cobbold J, Taylor-Robinson S, Marshall S, Orchard T. Differences in gut microbial metabolism are responsible for reduced hippurate synthesis in Crohn's disease. BMC Gastroenterology 2010, 10:108. 10.1186/1471-230X-10-108, 2954941, 20849615.
60. Barba I, de León G, Martín E, Cuevas A, Aguade S, Candell-Riera J, Barrabés JA, Garcia-Dorado D. Nuclear magnetic resonance-based metabolomics predicts exercise-induced ischemia in patients with suspected coronary artery disease. Magn Reson Med 2008, 60:27-32. 10.1002/mrm.21632, 18581408.